Reviews and perspectivesBeyond the FFA: The role of the ventral anterior temporal lobes in face processing
Introduction
Humans are an intrinsically social species. More sophisticated social-cognitive skills are thought to underlie human׳s advanced intelligence, our tremendous cultural advances, and the evolution of language (Dunbar and Shultz, 2007, Herrmann et al., 2007). Superior social skills in humans are driven, in part, by increased proficiency in the identification and discrimination of conspecifics. Humans are remarkably adept at face processing and have even been described as face processing “experts” as shown by extensive clinical and psychophysical research indicating that humans have specialized processes for recognizing faces that are distinct from those used for general object recognition (Farah et al., 1998, Gauthier and Tarr, 2002, Moscovitch et al., 1997). This expertise is supported by increased specialization in a number of cortical regions involved in face processing. Over a decade of neuroimaging work has characterized the neural basis of face perception and identified several nodes or ‘patches’ that preferentially respond to faces and ultimately contribute to humans׳ unique face processing proficiencies (Haxby et al., 2000, Kanwisher and Yovel, 2006).
Because there are multiple face patches, a natural question is whether there is redundancy in the code or whether any one region is critical for normal face processing abilities. Of the regions that respond to faces more than other objects, the fusiform face area (FFA), occipital face area (OFA), and posterior superior temporal sulcus (pSTS) are proposed to constitute the “core” face recognition system, whereas the ventral anterior temporal lobe (vATL) and the amygdala are part of the “extended network” for face recognition (Haxby et al., 2000, Rossion et al., 2003). This proposal has lead to the false presumption that the vATLs play a non-critical role in face processing. However several lines of evidence strongly suggest that the vATLs play a necessary role in face perception and identification. Indeed, face-processing deficits have been more reliably observed following damage to the vATLs than more posterior portions of the face-processing network (Heywood & Cowey, 1992). Furthermore, a small but emerging body of literature has shown that a region in the vATLs is selective for faces and is interconnected with the FFA and the OFA. Early imaging studies of face perception likely missed these face-selective activations in the ATLs because they used a restricted field-of-view that excluded the inferior temporal lobe from image acquisition, or because they suffered from the well known problem of imaging the ATLs: susceptibility artifacts and signal distortion due to the proximity of these regions to the nasal sinuses and ear canals (Devlin et al., 2000, Visser et al., 2010). However, recent findings of face-selective cortical areas—“face patches”—in the vATLs of monkeys have spurred fMRI researchers to optimize signal detection in the vATLs, resulting in several recent studies suggesting that functionally homologous face-processing areas may exist in the vATLs of humans (see Fig. 1a) (Avidan et al., 2014, Pinsk et al., 2009, Rajimehr et al., 2009, Tsao et al., 2008).
Here, we will review evidence suggesting that that the ventral ATLs play a critical role in face processing. We propose that a hierarchically organized system of face-selective patches extends bilaterally from the inferior occipital gyri to the vATLs and performs the visual computations necessary for accurate facial identification. As feed-forward processing proceeds along this network, facial representations become increasingly complex and abstracted from low-level perceptual features. We further speculate that a face-selective region of the vATLS, which we will refer to as the anterior temporal face area, is the apex of this hierarchy, serving to link viewpoint invariant face representations with person-specific semantic knowledge. In the following sections, we briefly review literature on the posterior face areas (OFA and FFA; see Fig. 2) in order to place our proposal in context. The remaining sections will focus on neuroimaging and neuropsychology literature implicating the vATLs in face processing, and will highlight a small but emerging body of work that has examined the response properties of a face-sensitive region within the vATLs, the anterior temporal face area (see Fig. 2 for an illustration of the brain regions mentioned in this review). Finally we will suggest additional modifications to current neural models of face processing.
Section snippets
The fusiform face area
A large body research has focused on the fusiform face area (FFA), located in the lateral middle fusiform gyrus (BA 37) which responds more strongly to faces than to other objects (Allison et al., 1999, Bentin et al., 1996, Halgren et al., 2000, Haxby et al., 1996, Kanwisher et al., 1997, Sergent et al., 1992). Face representations in the FFA are invariant to low-level stimulus manipulations such as position (Kovács, Cziraki, Vidnyánszky, Schweinberger, & Greenlee, 2008), size (Andrews and
The occipital face area
The OFA is located upstream from the FFA, on the inferior surface of the occipital gyrus (BA 19), and likely contributes to an earlier stage of face analysis than the FFA (Fairhall & Ishai, 2007). This region is primarily sensitive to low-level perceptual attributes of faces, such as spatial frequency (Eger et al., 2004), viewpoint (Ewbank & Andrews, 2008), and location (Kovács et al., 2008, Schwarzlose et al., 2008). The results from several studies have suggested that the OFA is responsible
Evidence from macaques
Single-unit recording studies have found face sensitive neurons on the inferior bank of the anterior STS, the anterior middle temporal gyrus (MTG), the temporal pole, and the inferior surface of the ATL (De Souza et al., 2005, Eifuku et al., 2004, Hasselmo et al., 1989, Ku et al., 2011, Leopold et al., 2006). Using high-resolution fMRI it has been shown that these cells are organized into six face-selective cortical areas (face-patches) on the macaque temporal lobe, each with different
Connectivity of the ventral anterior temporal face area
During the last decade, there has seen a strong emphasis on functional specialization of cortical regions and a relative disregard of structural connectivity as an explanation for various neurological syndromes. However diffusion imaging has reawakened interest in disconnection as a possible explanation for some disorders, including prosopagnosia. As reviewed earlier, there is evidence from macaques that face sensitive patches along the inferior temporal lobe form a tightly interconnected
Extending previous models of face processing
The focus of this review is the contribution of the vATLs to face processing. However we suggest two additional addendums to previous neural models of face perception that we outline below.
Conclusions
Haxby and colleagues (Gobbini and Haxby, 2007, Haxby et al., 2000) distinguish between a core system—the OFA, FFA, and pSTS—that encodes the visual appearance of a face and an extended system—the anterior temporal lobes, as well as several other limbic and non-limbic structures—responsible for processing the meaning of information derived from a face. Although these authors attribute the representation of biographical information to the anterior temporal lobes generally, they made no claims
Acknowledgments
We would like to thank Vanessa Troiani for assistance with conceptual aspects of this manuscript, and two anonymous reviewers for their very helpful insights on earlier versions of this manuscript. This work was funded by a National Institute of Health Grant to I. Olson [RO1 MH091113].
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